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Journal of Molecular Evolution

, Volume 86, Issue 3–4, pp 190–203 | Cite as

Horizontal Gene Transfer Building Prokaryote Genomes: Genes Related to Exchange Between Cell and Environment are Frequently Transferred

  • Apuã C. M. Paquola
  • Huma Asif
  • Carlos Alberto de Bragança Pereira
  • Bruno César Feltes
  • Diego Bonatto
  • Wanessa Cristina Lima
  • Carlos Frederico Martins Menck
Original Article

Abstract

Horizontal gene transfer (HGT) has a major impact on the evolution of prokaryotic genomes, as it allows genes evolved in different contexts to be combined in a single genome, greatly enhancing the ways evolving organisms can explore the gene content space and adapt to the environment. A systematic analysis of HGT in a large number of genomes is of key importance in understanding the impact of HGT in the evolution of prokaryotes. We developed a method for the detection of genes that potentially originated by HGT based on the comparison of BLAST scores between homologous genes to 16S rRNA-based phylogenetic distances between the involved organisms. The approach was applied to 697 prokaryote genomes and estimated that in average approximately 15% of the genes in prokaryote genomes originated by HGT, with a clear correlation between the proportion of predicted HGT genes and the size of the genome. The methodology was strongly supported by evolutionary relationships, as tested by the direct phylogenetic reconstruction of many of the HGT candidates. Studies performed with Escherichia coli W3110 genome clearly show that HGT proteins have fewer interactions when compared to those predicted as vertical inherited, an indication that the number of protein partners imposes limitations to horizontal transfer. A detailed functional classification confirms that genes related to protein translation are vertically inherited, whereas interestingly, transport and binding proteins are strongly enriched among HGT genes. Because these genes are related to the cell exchange with their environment, their transfer most likely contributed to successful adaptation throughout evolution.

Keywords

Horizontal gene transfer Evolution Phylogenetic tree incongruence Transport proteins 

Notes

Authors’ Contribution

AP, WL, and CM designed and developed the method. CM defined the strategy and supervised. HA, CP, BC, and DB analyzed the data. HA, AP, and CM wrote, discussed, and edited the manuscript. AP, HA, and BC prepared the figures. WL discussed and edited the manuscript.

Funding

This project received financial support from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Brasília, DF, Brazil) and Comissão de Aperfeiçoamento do Ensino Superior (CAPES, Brasília, DF, Brazil) and Foundation for Research Support of the State of Sao Paulo (FAPESP, São Paulo, SP, Brazil).

Compliance with Ethical Standards

Competing interests

The authors declare that they have no competing interests.

Supplementary material

239_2018_9836_MOESM1_ESM.docx (6.6 mb)
Supplementary material 1 (DOCX 6774 KB)
239_2018_9836_MOESM2_ESM.csv (60 kb)
Supplementary material 2 (CSV 59 KB)
239_2018_9836_MOESM3_ESM.txt (19 mb)
Supplementary material 3 (TXT 19439 KB)

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Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Apuã C. M. Paquola
    • 1
    • 2
  • Huma Asif
    • 1
    • 3
  • Carlos Alberto de Bragança Pereira
    • 4
  • Bruno César Feltes
    • 5
    • 6
  • Diego Bonatto
    • 5
  • Wanessa Cristina Lima
    • 1
    • 7
  • Carlos Frederico Martins Menck
    • 1
  1. 1.Department of Microbiology, Institute of Biomedical SciencesUniversity of Sao PauloSão PauloBrazil
  2. 2.Lieber Institute for Brain DevelopmentBaltimoreUSA
  3. 3.Department of Psychiatry and Behavioral NeurosciencesThe University of ChicagoChicagoUSA
  4. 4.Department of Statistics, Institute of Mathematics and StatisticsUniversity of Sao PauloSão PauloBrazil
  5. 5.Center of Biotechnology, Department of Molecular Biology and BiotechnologyFederal University of Rio Grande do SulPorto AlegreBrazil
  6. 6.Institute of Informatics, Structural Bioinformatics and Computational Biology LaboratoryFederal University of Rio Grande do SulPorto AlegreBrazil
  7. 7.Department of PharmacologyUniversity of HeidelbergHeidelbergGermany

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